β-Hairpin of Islet Amyloid Polypeptide Bound to an Aggregation Inhibitor

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Mirecka, Ewa A ^a   Feuerstein, Sophie ^b   Gremer, Lothar ^a,b   Schröder, Gunnar F ^a,b   Stoldt, Matthias ^a,b   Willbold, Dieter ^a,b   Hoyer, Wolfgang ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLIN; AMYLOID; AMYLOID BETA PROTEIN; PROTEIN AGGREGATE; PROTEIN BINDING; RECOMBINANT PROTEIN; SERINE;

AMINO ACID SEQUENCE; CHEMISTRY; DRUG EFFECT; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE;

ALPHA-SYNUCLEIN; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PEPTIDES; HUMANS; ISLET AMYLOID POLYPEPTIDE; MODELS, MOLECULAR; PROTEIN AGGREGATES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SERINE;

EID: 84988346218     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep33474     Document Type: Article

References (56)

1. Knowles, T. P., Vendruscolo, M. & Dobson, C. M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396 (2014).
2. Cao, P. et al. Islet amyloid: from fundamental biophysics to mechanisms of cytotoxicity. FEBS Lett. 587, 1106-1118 (2013).
3. Westermark, P., Andersson, A. & Westermark, G. T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795-826 (2011).
4. Jaikaran, E. T. et al. Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis. J. Mol. Biol. 308, 515-525 (2001).
5. Nielsen, J. T. et al. Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 48, 2118-2121 (2009).
6. Nilsson, M. R. & Raleigh, D. P. Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin. J. Mol. Biol. 294, 1375-1385 (1999).
7. Tenidis, K. et al. Identification of a penta-And hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J. Mol. Biol. 295, 1055-1071 (2000).
8. Westermark, P., Engstrom, U., Johnson, K. H., Westermark, G. T. & Betsholtz, C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc. Natl. Acad. Sci. USA 87, 5036-5040 (1990).
9. Alexandrescu, A. T. Amide proton solvent protection in amylin fibrils probed by quenched hydrogen exchange NMR. PLoS One 8, e56467 (2013).
10. Luca, S., Yau, W. M., Leapman, R. & Tycko, R. Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry 46, 13505-13522 (2007).
11. Andreetto, E. et al. A Hot-Segment-Based Approach for the Design of Cross-Amyloid Interaction Surface Mimics as Inhibitors of Amyloid Self-Assembly. Angew. Chem. Int. Ed. 54, 13095-13100 (2015).
12. Buchanan, L. E. et al. Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient β-sheet. Proc. Natl. Acad. Sci. USA 110, 19285-19290 (2013).
13. Hebda, J. A., Saraogi, I., Magzoub, M., Hamilton, A. D. & Miranker, A. D. A peptidomimetic approach to targeting preamyloidogenic states in type II diabetes. Chem. Biol. 16, 943-950 (2009).
14. Middleton, C. T. et al. Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor. Nat. Chem. 4, 355-360 (2012).
15. Young, L. M. et al. Screening and classifying small-molecule inhibitors of amyloid formation using ion mobility spectrometry-mass spectrometry. Nat. Chem. 7, 73-81 (2015).
16. Saunders, J. C. et al. An in vivo platform for identifying inhibitors of protein aggregation. Nat. Chem. Biol. 12, 94-101 (2016).
17. Mirecka, E. A. et al. Engineered aggregation inhibitor fusion for production of highly amyloidogenic human islet amyloid polypeptide. J. Biotechnol. 191, 221-227 (2014).
18. Grnwall, C. et al. Selection and characterization of Affibody ligands binding to Alzheimer amyloid β peptides. J. Biotechnol. 128, 162-183 (2007).
19. Hoyer, W., Grnwall, C., Jonsson, A., Sthl, S. & Hrd, T. Stabilization of a β-hairpin in monomeric Alzheimers amyloid-β peptide inhibits amyloid formation. Proc. Natl. Acad. Sci. USA 105, 5099-5104 (2008).
20. Shaykhalishahi, H. et al. A β-hairpin-binding protein for three different disease-related amyloidogenic proteins. ChemBioChem 16, 411-414 (2015).
21. Mirecka, E. A. et al. Sequestration of a β-hairpin for control of α-synuclein aggregation. Angew. Chem. Int. Ed. 53, 4227-4230 (2014).
22. Dupuis, N. F., Wu, C., Shea, J. E. & Bowers, M. T. Human islet amyloid polypeptide monomers form ordered β-hairpins: A possible direct amyloidogenic precursor. J. Am. Chem. Soc. 131, 18283-18292 (2009).
23. Reddy, A. S. et al. Stable and metastable states of human amylin in solution. Biophys. J. 99, 2208-2216 (2010).
24. Wu, C. & Shea, J. E. Structural similarities and differences between amyloidogenic and non-Amyloidogenic islet amyloid polypeptide (IAPP) sequences and implications for the dual physiological and pathological activities of these peptides. PLoS Comp. Biol. 9, e1003211 (2013).
25. Cao, P. et al. Sensitivity of amyloid formation by human islet amyloid polypeptide to mutations at residue 20. J. Mol. Biol. 421, 282-295 (2012).
26. Meier, D. T. et al. The S20G substitution in hIAPP is more amyloidogenic and cytotoxic than wild-Type hIAPP in mouse islets. Diabetologia (2016).
27. Sakagashira, S. et al. S20G mutant amylin exhibits increased in vitro amyloidogenicity and increased intracellular cytotoxicity compared to wild-Type amylin. Am. J. Pathol. 157, 2101-2109 (2000).
28. Xu, W., Jiang, P. & Mu, Y. Conformation preorganization: effects of S20G mutation on the structure of human islet amyloid polypeptide segment. J. Phys. Chem. B 113, 7308-7314 (2009).
29. Padrick, S. B. & Miranker, A. D. Islet amyloid polypeptide: identification of long-range contacts and local order on the fibrillogenesis pathway. J. Mol. Biol. 308, 783-794 (2001).
30. Marek, P. et al. Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 46, 3255-3261 (2007).
31. Porat, Y., Mazor, Y., Efrat, S. & Gazit, E. Inhibition of islet amyloid polypeptide fibril formation: A potential role for heteroaromatic interactions. Biochemistry 43, 14454-14462 (2004).
32. Andreetto, E. et al. Identification of hot regions of the Aβ-IAPP interaction interface as high-Affinity binding sites in both cross-And self-Association. Angew. Chem. Int. Ed. 49, 3081-3085 (2010).
33. ONuallain, B., Williams, A. D., Westermark, P. & Wetzel, R. Seeding specificity in amyloid growth induced by heterologous fibrils. J. Biol. Chem. 279, 17490-17499 (2004).
34. Bachhuber, T. et al. Inhibition of amyloid-β plaque formation by α-synuclein. Nat. Med. 21, 802-807 (2015).
35. Serrano-Pozo, A., Frosch, M. P., Masliah, E. & Hyman, B. T. Neuropathological alterations in Alzheimer disease. Cold Spring Harbor perspectives in medicine 1, a006189 (2011).
36. Guo, J. L. et al. Distinct α-synuclein strains differentially promote tau inclusions in neurons. Cell 154, 103-117 (2013).
37. Yang, Y. & Song, W. Molecular links between Alzheimers disease and diabetes mellitus. Neuroscience 250, 140-150 (2013).
38. Jackson, K. et al. Amylin deposition in the brain: A second amyloid in Alzheimer disease? Ann. Neurol. 74, 517-526 (2013).
39. Oskarsson, M. E. et al. In vivo seeding and cross-seeding of localized amyloidosis: A molecular link between type 2 diabetes and Alzheimer disease. Am. J. Pathol. 185, 834-846 (2015).
40. Yan, L. M., Velkova, A., Tatarek-Nossol, M., Andreetto, E. & Kapurniotu, A. IAPP mimic blocks Aβ cytotoxic self-Assembly: crosssuppression of amyloid toxicity of Aβ and IAPP suggests a molecular link between Alzheimers disease and type II diabetes. Angew. Chem. Int. Ed. 46, 1246-1252 (2007).
41. Young, L. M. et al. Insights into the consequences of co-polymerisation in the early stages of IAPP and Abeta peptide assembly from mass spectrometry. Analyst 140, 6990-6999 (2015).
42. Lendel, C. et al. A hexameric peptide barrel as building block of amyloid-β protofibrils. Angew. Chem. Int. Ed. 53, 12756-12760 (2014).
43. Sandberg, A. et al. Stabilization of neurotoxic Alzheimer amyloid-β oligomers by protein engineering. Proc. Natl. Acad. Sci. USA 107, 15595-15600 (2010).
44. McCluskey, J. T. et al. Development and functional characterization of insulin-releasing human pancreatic beta cell lines produced by electrofusion. J. Biol. Chem. 286, 21982-21992 (2011).
45. Zraika, S. et al. Toxic oligomers and islet beta cell death: guilty by association or convicted by circumstantial evidence? Diabetologia 53, 1046-1056 (2010).
46. Larson, J. L. & Miranker, A. D. The mechanism of insulin action on islet amyloid polypeptide fiber formation. J. Mol. Biol. 335, 221-231 (2004).
47. Dupuis, N. F., Wu, C., Shea, J. E. & Bowers, M. T. The amyloid formation mechanism in human IAPP: dimers have β-strand monomer-monomer interfaces. J. Am. Chem. Soc. 133, 7240-7243 (2011).
48. Shim, S. H. et al. Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residuespecific resolution. Proc. Natl. Acad. Sci. USA 106, 6614-6619 (2009).
49. Delaglio, F. et al. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
50. Vranken, W. F. et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696 (2005).
51. Solyom, Z. et al. BEST-TROSY experiments for time-efficient sequential resonance assignment of large disordered proteins. J. Biomol. NMR 55, 311-321 (2013).
52. Cheung, M. S., Maguire, M. L., Stevens, T. J. & Broadhurst, R. W. DANGLE: A Bayesian inferential method for predicting protein backbone dihedral angles and secondary structure. J. Magn. Reson. 202, 223-233 (2010).
53. Brunger, A. T. Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733 (2007).
54. Rieping, W. et al. ARIA2: Automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23, 381-382 (2007).
55. Cohen, S. I. et al. Nucleated polymerization with secondary pathways. I. Time evolution of the principal moments. J. Chem. Phys. 135, 065105 (2011).
56. Meisl, G. et al. Molecular mechanisms of protein aggregation from global fitting of kinetic models. Nat. Protoc. 11, 252-272 (2016).